Vol. 13(3), pp. 184-191, July-September 2021 DOI: 10.5897/JPHE2021.1332 Article Number: D5518AA67362 ISSN: 2141-2316 Copyright©2021 Author(s) retain the copyright of this article Journal of Public Health and Epidemiology http://www.academicjournals.org/JPHE

Full Length Research Paper

Integrated approach in the control of neglected tropical diseases with cutaneous manifestations in four municipalities in : A cross-sectional study

Parfait DJOSSOU1*, Ghislain Emmanuel SOPOH2, Ronald Sètondji GNIMAVO2, Esaï Gimatal ANAGONOU3, Zoulkifl Salou BACHIROU1, Franck Zinsou Maurille MIGNANWANDE1, Horace DEGNONVI1, Flora Sylvie HOUNDJREBO4, Jean Gabin HOUEZO3, Akpéédjé Carolle WADAGNI3, Yves Thierry BAROGUI3 and Roch Christian JOHNSON1

1Centre Interfacultaire de Formation et de Recherche en Environnement pour le Développement Durable, Université d’-Calavi, Bénin. 2Institut Régional de Santé Publique-Comlan Alfred QUENUM, , Université d’Abomey-Calavi, Bénin. 3Programme National de Lutte contre la Lèpre et l’Ulcère de Buruli, Ministère de la Santé, Bénin. 4Laboratoire d’Anthropologie Médicale Appliquée, Université d’Abomey-Calavi, Bénin.

Received 24 May, 2021; Accepted 19 July, 2021

The integrated approach is the new recommendation of the World Health Organization (WHO) for the control of neglected tropical diseases. The goal of this cross-sectional study was to implement this approach in 4 municipalities with a high prevalence of leprosy in Benin from September 2019 to August 2020. Mobile medical consultations were organized in these municipalities following the mobilization and sensitization of the populations. In the 4 municipalities, 6416 people were examined. The mean age was (27.3 ±19.8) years. Women represented 52.7% of people examined. Among the 6416 people examined, 1230 (19.2%) had skin conditions. The most common skin conditions were pityriasis versicolor (421 cases; 34.2%); eczema (203 cases; 16.5%); ringworm (159 cases; 12.9%); pruritus sine materia (81 cases; 6.6%); acne (62 cases; 5.0%); epidermophytia (37 cases; 3.0%); achromic nevus (35 cases; 2.8%); keloids (28 cases; 2.3%); chronic ulcers (27 cases; 2.2%) and depigmentation stigmata (24 cases; 2.0%). 8 new leprosy cases (0.7%) were detected. This study proves the efficiency of the integrated approach in the control of neglected tropical diseases (NTDs) with cutaneous manifestations in Benin.

Key words: Neglected tropical disease, leprosy, skin disease, integration, disease control, Benin.

INTRODUCTION

The skin is the most visible structural element both for personal and social well-being of the patient. The skin is patients and caregivers who examine them. Any skin therefore an important point of intervention for both condition is noticeable and will have an effect on the diagnostic and therapeutic procedures (OMS, 2018a).

*Corresponding author. E-mail: [email protected].

Author(s) agree that this article remain permanently open access under the terms of the Creative Commons Attribution License 4.0 International License

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Many neglected tropical diseases (NTDs) affect the municipalities of , , and Kétou. skin, causing considerable disability, stigma and exacerbation of poverty (Engelman et al., 2016). NTDs Participants cause changes in the skin, with symptoms ranging from pruritus to changes in colour, feeling or appearance A non-probabilistic method in conjunction with a convenience- (OMS, 2018a). In addition, NTDs with cutaneous based choice technique was used in this study. Thus, any person who was at least 1 year old, available and who gave consent after manifestations are co-endemic in many countries, districts being informed, was included in the study. For participants under 18 and communities (Amazigo, 2008; Alvar et al., 2012; van years old, the consent of parents or guardians has been requested. de Sande, 2013; Mitjà et al., 2014; WHO, 2014; Mitjà et al., 2015; Yotsu et al., 2015; WHO, 2016). These cutaneous NTDs are responsible for the loss of a large number of Data collection disability-adjusted life years (DALY) (WHO, 2010). Social mobilization was carried out in the 96 villages by community Integrating efforts to control cutaneous NTDs can health volunteers, local elected officials and town criers. Information facilitate progress in understanding and controlling this sessions on skin diseases, especially leprosy, were organized for diverse group of diseases (Engelman et al., 2016). the participants. Thus, the purpose and benefits of the study were Indeed, examination of the skin offers the opportunity to presented each time at the start of consultations in the villages where the study was conducted. The consultations were done in screen individuals in communities or children in schools public places, sometimes in schools, in rooms well-lit by daylight to identify multiple conditions in a single visit. This while respecting the patients’ privacy. Two teams were formed, common approach for controlling these skin diseases each composed a leprosy specialist/dermatologist, a local health justifies the integrated delivery of health care worker and a data collection agent. When a person, after being interventions to both increase cost-effectiveness and informed of the objectives of the study, agrees to participate, he/she expand coverage (Mitjà et al., 2017). is examined by a leprosy specialist/dermatologist. This latter looked for the cardinal signs of leprosy and for symptoms of Buruli ulcers In Benin, two programmes have been involved in the (BU) and yaws on the participant's body. In addition, the leprosy control of NTDs. The National Program for the Control of specialist/dermatologist looked for signs of other dermatoses (OMS, Neglected Tropical Diseases (PNLMTN) is engaged in 2018b). The leprosy specialists/dermatologists were helped by local the treatment of NTDs in general, whereas the National health workers and data collectors who were responsible for Program for the Control of Leprosy and Buruli Ulcers providing out dermatological drugs and filling out data collection (PNLLUB) addresses only cutaneous NTDs including forms. Thus, the sociodemographic information and data on the characteristics of the skin conditions were collected. Leprosy Buruli ulcers, leprosy and yaws. Despite the efforts of screening was carried out by leprosy specialists/dermatologists these programmes, NTDs in general and those with according to the WHO clinical criteria. The leprosy patients were cutaneous manifestations in particular persist. Many clinically diagnosed according to the WHO clinical definitions. The challenges remain for these programmes, especially patients were classified as paucibacillary (≤ 5 lesions) or PNLLUB, in achieving the control of Buruli ulcers and multibacillary (> 5 lesions or with nerve enlargement) according to the WHO classification (Géniaux, 2010; OMS, 2016). All leprosy yaws, the elimination of leprosy and the management new cases detected were systematically placed on multidrug and/or intensive care of the other cutaneous NTDs. The therapy (MDT). After receiving the first supervised dose of MDT, purpose of this study was to implement integrated these patients were referred to the municipality’s Leprosy Nursing approach for the control of NTDs with cutaneous Supervisor and the most accessible responsible health worker. manifestations in the municipalities of Djidja, Ouinhi, These patients benefited the disability prevention counselling Zagnanado and Kétou in Benin. sessions too. Some were given shea butter for the care of scars and the prevention of dry skin. The contacts of new leprosy cases were systematically examined too. In addition, the non-leprosy patients were carefully assessed by the leprosy specialists/ MATERIALS AND METHODS dermatologists to determine the type of dermatosis and the appropriate treatment. An appropriate treatment was given to each Study framework type of dermatosis diagnosed. The necessary inputs for bandages and dressings were also made available to patients with chronic The study was conducted in 96 villages of the municipalities of ulcers. These patients were then referred to the nearest BU Djidja, Ouinhi, Zagnanado (in the department of Zou) and Kétou (in treatment centres. the department of Plateau) in Benin (Figure 1). These municipalities were selected according to the endemicity of leprosy (PNLLUB, 2019). The estimated populations of these municipalities were Variables respectively 146,681, 70,507, 65,377 and 186,834 inhabitants for Djidja, Ouinhi, Zagnanado and Kétou (INSAE, 2016). The variable of interest was the skin condition diagnosed through the presence of clinical signs. The sociodemographic informations such as age and gender were recorded for each person examined.

Study design and population Data processing and statistical analysis This is a cross-sectional study carried out from September 2019 to August 2020. It was conducted on the populations of the The data collected in the field were recorded using Microsoft Excel

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Figure 1. Municipalities and villages investigated in the study.

2016 and analysed with IBM SPSS 25. Proportions were calculated (159 cases; 12.9%); pruritus sine materia (81 cases; for the different skin conditions detected and for the other 6.6%); acne (62 cases; 5.0%); epidermophytia (37 cases; qualitative variable (gender). The mean and standard deviation 3.0%); achromic nevus (35 cases; 2.8%); keloids (28 were determined for the quantitative variable (age). cases; 2.3%); chronic ulcers (27 cases; 2.2%) and depigmentation stigmata (24 cases; 2.0%) (Table 2). Ethical aspects Some of these conditions are presented in Figure 2a to i. Among the 6416 persons examined, 8 new leprosy This study was authorized by the National Ethics Committee for cases were detected. Of these patients, 4 were from the Health Research (CNERS) of the Ministry of Health Benin (ethical authorization N°21/MS/DC/SGM/DRFMT/CNERS/SA). Informed municipality of Djidja, 2 were from the municipality of consent was obtained from each participant before any data Ouinhi and 2 were from the municipality of Zagnanado. collection. Of these cases, 4 were multibacillary, 4 were paucibacillary and none of them had any disability. One was a paediatric paucibacillary case (14 years old). RESULTS These cases systematically received the first supervised dose of multidrug therapy (MDT) and were referred to the The study mobilized 9,941 people. A total of 6416 most accessible municipality’s Leprosy Nursing (64.5%) had given their consent to be examined. The Supervisor and the responsible health worker. mean age was (27.3 ±19.8) years and the women represented 52.7% (Table 1). The reasons that 3,525 people did not participate in the study included lack of DISCUSSION consent, refusal to be examined and to wait. Of the 6416 participants examined, 1230 (19.2%) had Using integrated approach of screening for skin diseases, at least one skin condition (502 people in Djidja, 322 in this study confirmed the endemicity of leprosy in the Ouinhi, 241 in Zagnanado and 165 in Kétou). The most municipalities of Djidja, Ouinhi, Zagnanado and Kétou in common skin conditions were pityriasis versicolor (421 Benin and helped to detect and treat many other skin cases; 34.2%); eczema (203 cases; 16.5%); ringworm diseases. The mean age of the participants was (27.3 ±

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Table 1. Socio-demographic characteristics of the people examined.

Djidja Ouinhi Zagnanado Characteristics Kétou (n=801) Total (n=6416) (n=2472) (n=1579) (n=1564) Age Mean (standard deviation) 23.7(±19.8 30.5(±19.6) 31.6(±21.1) 23.6(±18.7) 27.3(±19.8)

Gender Male (%) 1151 (46.6) 775 (49.1) 709 (45.3) 400 (49.9) 3035 (47.3) Female (%) 1321 (53.4) 804 (50.9) 855 (54.7) 401 (50.1) 3381 (52.7)

Table 2. Diagnosed skin conditions.

Skin conditions Djidja Ouinhi Zagnanado Kétou Total (N) Total (%) Infectious diseases

Fungal conditions

Total 250 181 119 80 630 51.2

Seborrheic dermatitis 1 0 0 0 1 0.1 Epidermophytia 22 8 4 3 37 3.0 Mycotic intertrigo 2 2 1 2 7 0.6 Onychomycosis 3 0 0 2 5 0.4 Pityriasis versicolor (PV) 127 156 101 37 421 34.2 Ringworm 95 15 13 36 159 12.9

Bacterial diseases

Total 7 5 5 5 22 1.8 Abscess 0 1 3 5 9 0.7 Erysipelas 1 0 0 0 1 0.1 Furuncle 1 0 0 0 1 0.1 Leprosy 4 2 2 0 8 0.7 Impetigo 0 2 0 0 2 0.2 Syphilis 1 0 0 0 1 0.1

Viral conditions

Total 2 2 1 0 5 0.4 Pityriasis Rosea of Gibert (PRG) 1 2 1 0 4 0.3 Shingles 1 0 0 0 1 0.1

Parasitic conditions

Total 10 3 1 6 20 1.6 Scabies 10 3 1 6 20 1.6

No infectious conditions

Immuno-allergic conditions

Total 140 49 62 48 299 24.3 Eczema 85 39 44 35 203 16.5 Fixed erythema pigmentosum toxicosis 1 4 1 0 6 0.5 Prurigo strophulus 1 1 0 1 3 0.2 Pruritus sine materia 51 2 16 12 81 6.6 Urticaria 2 3 1 0 6 0.5

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Table 2. Contd.

Inflammatory conditions

Total 37 11 11 7 66 5.4 Acne 35 9 11 7 62 5.0 Cutaneous lichen 0 1 0 0 1 0.1 Lupus 2 1 0 0 3 0.2

Tumor or pseudotumor conditions

Total 7 26 9 5 47 3.8 Fibrosing Folliculitis 4 2 4 4 14 1.1 Keloids 3 19 5 1 28 2.3 Lipoma 0 2 0 0 2 0.2 Neurofibromatosis 0 3 0 0 3 0.2

Other conditions

Total 49 45 33 14 141 11.5 Achromic nevus 12 16 7 0 35 2.8 Chronic ulcer 5 13 3 6 27 2.2 Crystal miliaria 0 0 1 2 3 0.2 Cutaneous xerosis 2 1 0 0 3 0.2 Lymphedema 3 3 3 0 9 0.7 Plantar Keratoderma 12 0 0 1 13 1.1 Stigma of depigmentation 6 4 11 3 24 2.0 Unsightly scar 5 6 8 1 20 1.6 Vitiligo 4 2 0 1 7 0.6 Total 502 322 241 165 1230 100.0

19.8) years with a predominance of women. These one reported in one study conducted in an Indian village, results reflected the situation at the national level where which reported a prevalence of 11.16% (Rao and Kumar women predominate in the Beninese population (INSAE, 2003). This result was also higher than the one obtained 2016). These findings corroborate the results of one in Côte d'Ivoire, which reported a prevalence of 15.0% study that showed that women and children are the most (Koffi et al., 2020). On the other hand, this proportion was vulnerable and most affected by neglected tropical much lower than the 64.5% reported in a study diseases (Hotez et al., 2007). Our results were also conducted in Munich (Tizek et al., 2019). Our prevalence consistent with those of a study conducted on sex and is also lower than the one obtained in a community-based age adjusted prevalence estimates of five chronic clinical skin examination of 400 subjects in 4 villages in inflammatory skin diseases in France where it was found Cameroon and one other obtained in literature review a strong representation of the female gender (Richard et study where the overall prevalence of school children al., 2018). A similarity was observed in a study carried with skin disease was 34.6 and 42.0% in two Ghanaian out on the prevalence of skin diseases in an outpatient studies, 45.8% in Gabon and 26.7% in Rwanda (Bissek dermatology clinic in Turkey (Bilgili et al., 2013). On the et al., 2012; Hogewoning et al., 2013). The difference in other hand, our results were inconsistent with those results could be explained by the diversity of targets, obtained in a study of 3673 patients attending a medical sample size and screening technique. camp in Kumble, India, which revealed a predominance In the present study, the most common skin conditions of the male sex (Rao and Kumar, 2003). This difference were pityriasis versicolor (34.2%); eczema, ringworm, in results may be related to the target population, sample pruritus sine materia, acne, epidermophytia, achromic size, and screening technique. Our study focused on nevus, keloids, chronic ulcers and depigmentation mobile consultations whereas this study involved stigmata. All skin conditions cases received appropriate consultations in a hospital. This could mean that the treatment using dermatological drugs. These results are mobile strategy improves accessibility for women and similar to those reported at Nepal, Yucatan (Mexico) and reduces gender-based inequities. Laos (Walker et al., 2008; Paek et al., 2012; Wootton et Our results showed that among the participants, 19.2% al., 2018). Among the participants, 8 new leprosy cases had skin conditions. This prevalence is higher than the were detected representing 0.7% of skin conditions (4

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Figure 2. Diagnosed skin conditions (a: Pityriasis versicolor b: Ringworm, c: Epidermophytia d: Neurofibromatosis of type 1 e: Cutaneous lichen f: Keloids g: Lupus vitiligoides h: Chronic ulcer h: Shingles).

cases of multibacillary and 4 cases of paucibacillary consultations in these communities. These leprosy form). This percentage was slightly higher than the 0.3% patients, fortunately diagnosed without visible reported one study conducted in the district of Lalo in deformities, were administered MDT to ensure proper Benin (Barogui et al., 2018). The number of leprosy healing due to the implementation of the integrated cases detected in our study is higher than that reported in approach. a study conducted in a regional hospital center in Burkina Despite the results in this study, it has several Faso who found 5 leprosy cases (Korsaga et al., 2018). limitations. One limitation is the use of the reasoned However, our percentage was lower than that reported choice technique (non-probability method), which in a study conducted in Côte d'Ivoire (Koffi et al., 2020). prevents us from generalizing our results to a larger The divergence in the results may be due to the population. Another limitation is the absence of an difference in study populations and sample sizes. established dermatologist in the screening team. This Our study also resulted in the early detection of 8 cases limitation is related to the scarcity of dermatologists in of leprosy, including a 14-year-old girl. This paediatric Benin (about 15). Nevertheless, skin conditions patient reflects recent transmission of leprosy in the study diagnosed in the field were assessed by dermatologists communities and thus represents a warning sign to to minimize nomenclature bias. Another limitation of our increase epidemiological surveillance of leprosy and to study is the organization of community-based fairground further promote active screening during mobile consultations that may constitute a barrier to participation

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in the study for some individuals with ugly lesions may be (APOC). Annals of Tropical Medicine and Parasitology 102(sup1):19- ashamed to show themselves in public (Sermrittirong et 22. Barogui YT, Diez G, Anagonou E, Johnson RC, Gomido IC, Amoukpo al., 2015; Hofstraat and van Brakel, 2016). Finally, the H, Bachirou ZS, Houezo JG, Saizonou R, Sopoh GE (2018). exclusively community-based clinic in the present study Integrated approach in the control and management of skin neglected could result in many children, especially school children, tropical diseases in Lalo, Benin. PLoS Neglected Tropical Diseases being missed during screening. It would then be 12(6):e0006584. Bilgili ME, Yildiz H, Sarici G (2013). Prevalence of skin diseases in a important to use the integrated approach by combining dermatology outpatient clinic in Turkey. A cross-sectional, community and school surveys. This was done by retrospective study. Journal of Dermatological Case Reports 7(4):108 researchers in Cameroon who successfully combined Bissek A-CZ-K, Tabah EN, Kouotou E, Sini V, Yepnjio FN, Nditanchou community and school-based surveys for the detection of R, Nchufor RN, Defo D, Dema F, Fonsah JY, Njamnshi AK, Muna WF (2012). The spectrum of skin diseases in a rural setting in Buruli ulcer and yaws (Boock et al., 2017). Cameroon (sub-Saharan Africa). BMC Dermatology 12(1):7 https://doi.org/10.1186/1471-5945-12-7 Boock AU, Awah PK, Mou F, Nichter M (2017). Yaws resurgence in Bankim, Cameroon: The relative effectiveness of different means of Conclusion detection in rural communities. PLoS neglected tropical diseases 11(5):e0005557. The integrated approach in the control of neglected Engelman D, Fuller LC, Solomon AW, McCarthy JS, Hay RJ, Lammie tropical diseases with cutaneous manifestations was PJ, Steer AC (2016). 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